Abstract
Biofloc technology has been applied successfully in the intensive aquaculture of several fish and shrimp species. The growth of heterotrophic microorganisms can be stimulated through adding extra carbon, which reduces the nitrogen level in the water and provides microbial protein to the animals. However, most of the studies and practical applications have been conducted in freshwater and marine environment. This paper focused on brine shrimp Artemia that lives in high salinity environment together with other halophilic or halotolerant microorganisms. The effect of carbon supplementation on Artemia growth, water quality, and microbial diversity of bioflocs was studied in the closed culture condition without any water exchange. The salinity of the culture medium was 100. A 24-d culture trial was conducted through supplementing sucrose at carbon/nitrogen (C/N) ratio of 5, 15, and 30 (Su5, Su15, and Su30), respectively. The culture without adding sucrose was used as a control. Artemia was fed formulated feed at a feeding ration of 60% recommended feeding level. The results showed that sucrose supplementation at higher C/N ratio (15 and 30) significantly improved the Artemia survival, growth and water quality (P<0.05). Addition of sucrose at C/N ratio of 15 and 30 significantly increased biofloc volume (BFV) (P<0.05). The Illumina MiSeq sequencing analysis showed that supplementing carbon at C/N ratio of 15 had a better total bacterial diversity and richness, and shaped the microbial composition at genera level. This study should provide information for studying the mechanism of biofloc technology and its application in high salinity culture conditions.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Asaduzzaman M, Wahab M A, Verdegem M C J, Huque S, Salam M A, Azim M E. 2008. C/N ratio control and substrate addition for periphyton development jointly enhance freshwater prawn Macrobrachium rosenbergii production in ponds. Aquaculture, 280(1–4): 117–123, https://doi.org/10.1016/j.aquaculture.2008.04.019.
Avnimelech Y. 1999. Carbon/nitrogen ratio as a control element in aquaculture systems. Aquaculture, 176(3–4): 227–235, https://doi.org/10.1016/S0044-8486(99)00085-X.
Avnimelech Y. 2006. Bio-filters: the need for an new comprehensive approach. Aquacultural Engineering, 34(3): 172–178, https://doi.org/10.1016/j.aquaeng.2005.04.001.
Azim M E, Little D C, Bron J E. 2008. Microbial protein production in activated suspension tanks manipulating C:N ratio in feed and the implications for fish culture. Bioresource Technology, 99(9): 3 590–3 599, https://doi.org/10.1016/j.biortech.2007.07.063.
Ballester E L C, Abreu P C, Cavalli R O, Emerenciano M, de Abreu L, Wasielesky JR W. 2010. Effect of practical diets with different protein levels on the performance of Farfantepenaeus paulensis juveniles nursed in a zero exchange suspended microbial flocs intensive system. Aquaculture Nutrition, 16(2): 163–172, https://doi.org/10.1111/j.1365-2095.2009.00648.x.
Bellisario B, Carere C, Cerfolli F, Angeletti D, Nascetti G, Cimmaruta R. 2013. Infaunal macrobenthic community dynamics in a manipulated hyperhaline ecosystem: a long-term study. Aquatic Biosystems, 9: 20, https://doi.org/10.1186/2046-9063-9-20.
Bowman J P, McMeekin T A. 2015. Alteromonas. In: Whitman W B ed. Bergey’s Manual of Systematics of Archaea and Bacteria. John Wiley & Sons, Ltd., New York.
Briones A, Raskin L. 2003. Diversity and dynamics of microbial communities in engineered environments and their implications for process stability. Current Opinion in Biotechnology, 14(3): 270–276, https://doi.org/10.1016/S0958-1669(03)00065-X.
Caporaso J G, Kuczynski J, Stombaugh J, Bittinger K, Bushman F D, Costello E K, Fierer N, Peña A G, Goodrich J K, Gordon J I, Huttley G A, Kelley S K, Knights D, Koenig J E, Ley R E, Lozupone C A, McDonald D, Muegge D B, Pirrung M, Reeder J, Sevinsky J R, Turnbaugh P J, Walters W A, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5): 335–336, https://doi.org/10.1038/nmeth.f.303.
Cardona E, Gueguen Y, Magré K, Lorgeoux B, Piquemal D, Pierrat F, Noguier F, Saulnier D. 2016. Bacterial community characterization of water and intestine of the shrimp Litopenaeus stylirostris in a biofloc system. BMC Microbiology, 16: 157e, https://doi.org/10.1186/s12866-016-0770-z.
Chirife J, Herszage L, Joseph A, Kohn E S. 1983. In vitro study of bacterial growth inhibition in concentrated sugar solutions: microbiological basis for the use of sugar in treating infected wounds. Antimicrobial Agents and Chemotherapy, 23(5): 776–773, https://doi.org/10.1128/AAC.23.5.766.
Crab R, Kochva M, Verstraete W, Avnimelech Y. 2009. Bioflocs technology application in over-wintering of tilapia. Aquacultural Engineering, 40(3): 105–112, https://doi.org/10.1016/j.aquaeng.2008.12.004.
Deng M, Chen J Y, Hou J, Li D P, He X G. 2017. The effect of different carbon sources on water quality, microbial community and structure of biofloc systems. Aquaculture, 482: 103–110, https://doi.org/10.1016/j.aquaculture.2017.09.030.
Ebeling J M, Timmons M B, Bisogni J J. 2006. Engineering analysis of the stoichiometry of photoautotrophic, autotrophic, and heterotrophic removal of ammonianitrogen in aquaculture systems. Aquaculture, 257(1–4): 346–358, https://doi.org/10.1016/j.aquaculture.2006.03.019.
Edgar R C, Haas B J, Clemente J C, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27(16): 2 194–2 200, https://doi.org/10.1093/bioinformatics/btr381.
Edgar R C. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10(10): 996–998, https://doi.org/10.1038/nmeth.2604.
Emerenciano M, Ballester E L C, Cavalli R O, Wasielesky W. 2012. Biofloc technology application as a food source in a limited water exchange nursery system for pink shrimp Farfantepenaeus brasiliensis (Latreille, 1817). Aquaculture Research, 43(3): 447–457, https://doi.org/10.1007/s10499-010-9408-6.
Gao M R, Wang J, Ma G N, Van Stappen G, Sui L Y. 2017. Carbon supplementation and microbial management to stimulate Artemia biomass production in hypersaline culture conditions. Aquaculture Research, 48(3): 1 240–1 250, https://doi.org/10.1111/are.12965.
Haas B J, Gevers D, Earl A M, Feldgarden M, Ward D V, Giannoukos G, Ciulla D, Tabbaa D, Highlander S K, Sodergren E, Methé B, De Santis T Z, Petrosino J F, Knight R, Birren B W. 2011. Chimeric 16s rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Research, 21(3): 494–504, https://doi.org/10.1101/gr.112730.110.
Hargreaves J A. 2006. Photosynthetic suspended-growth systems in aquaculture. Aquacultural Engineering, 34(3): 344–363, https://doi.org/10.1016/j.aquaeng.2005.08.009.
Kersters K, De Vos P, Gillis M, Swings J, Vandamme P, Stackebrand E. 2006. Introduction to the proteobacteria. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K H eds. The Prokaryotes. Springer, New York, NY. p.3–37, https://doi.org/10.1007/0-387-30745-1_1.
Labrenz M, Lawson P A, Tindall B J, Collins M D, Hirsch P. 2003. Saccharospirillum impatiens gen. nov., sp. nov., a novel γ-proteobacterium isolated from hypersaline Ekho Lake (East Antarctica). International Journal of Systematic and Evolutionary Microbiology, 53(3): 653–660, https://doi.org/10.1099/ijs.0.02406-0.
Lopes-dos-Santos R M A, Groot R, Sui L Y, Bossier P, Van Stappen G. 2019. Halophilic bacteria as a food source for the brine shrimp Artemia. Aquaculture, 500: 631–639, https://doi.org/10.1016/j.aquaculture.2018.10.068.
Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime J P, Hector A, Hooper D U, Huston M A, Raffaelli D, Schmid B, Tilman D, Wardle D A. 2001. Biodiversity and ecosystem functioning: current knowledge and future challenges. Science, 294(5543): 804–808, https://doi.org/10.1126/science.1064088.
Rahmani R, Zarrini G, Aein F, Hosseingholi E Z. 2016. Identification of extremely halophilic archaea associated with adult Artemia urmiana. Microbiology, 85(3): 386–388, https://doi.org/10.1134/S0026261716030127.
Ray A J, Lotz J M. 2014. Comparing a chemoautotrophic-based biofloc system and three heterotrophic-based systems receiving different carbohydrate sources. Aquacultural Engineering, 63: 54–61, https://doi.org/10.1016/j.aquaeng.2014.10.001.
Ronald L, Van Stappen G, Van Hoa N, Sorgeloos P. 2014. Effect of carbon/nitrogen ratio manipulation in feed supplements on Artemia production and water quality in solar salt ponds in the Mekong delta, Vietnam. Aquaculture Research, 45(12): 1 906–1 912, https://doi.org/10.1111/are.12135.
Santos M, Teixeira J, Rodrigues A. 2000. Production of dextransucrase, dextran and fructose from sucrose using Leuconostoc mesenteroides NRRL B512 (f). Biochemical Engineering Journal, 4(3): 177–188, https://doi.org/10.1016/S1369-703X(99)00047-9.
Schloss P D, Westcott S L, Ryabin T, Hall J R, Hartmann M, Hollister E B, Lesniewski R A, Oakley B B, Parks D H, Robinson C J, Sahl J W, Stres B, Thallinger G G, Van Horn D J, Weber C F. 2009. Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75(23): 7 537–7 541, https://doi.org/10.1128/AEM.01541-09.
Schveitzer R, Arantes R, Costódio P F S, do Espírito Santo C M, Arana L V, Seiffert W Q, Andreatta E R. 2013. Effect of different biofloc levels on microbial activity, water quality and performance of Litopenaeus vannamei in a tank system operated with no water exchange. Aquacultural Engineering, 56: 59–70, https://doi.org/10.1016/j.aquaeng.2013.04.006.
SOA. 2008. GB/T 12763.4-2007. Specifications for oceanographic survey, Part 4: survey of chemical parameters in sea water. Beijing: Standards Press of China. 75p. (in Chinese)
Sorgeloos P, Dhert P, Candreva P. 2001. Use of the brine shrimp, Artemia spp., in marine fish larviculture. Aquaculture, 200(1–2): 147–159, https://doi.org/10.1016/S0044-8486(01)00698-6.
Sui L Y, Wang J, Nguyen V H, Sorgeloos P, Bossier P, van Stappen G. 2013. Increased carbon and nitrogen supplementation in Artemia, culture ponds results in higher cyst yields. Aquaculture International, 21(6): 1 343–1 354, https://doi.org/10.1007/s10499-013-9637-6.
Toi H T, Boeckx P, Sorgeloos P, Bossier P, Van Stappen G. 2013. Bacteria contribute to Artemia nutrition in algae-limited conditions: a laboratory study. Aquaculture, 388–391: 1–7, https://doi.org/10.1016/j.aquaculture.2013.01.005.
Tovar A, Moreno C, Mánuel-Vez M P, García-Vargas M. 2000. Environmental impacts of intensive aquaculture in marine waters. Water Research, 34(1): 334–342, https://doi.org/10.1016/S0043-1354(99)00102-5.
Van Stappen G. 1996. Use of cysts. In: Lavens P, Sorgeloos P eds. Manual on the Production and Use of Live Food for Aquaculture. FAO, Rome, Italy. p.107–136.
Van Stappen G. 2002. Zoogeography. In: Abatzopoulos T J, Beardmore J A, Clegg J S, Sorgeloos P eds. Artemia: Basic and Applied Biology. Kluwer Academic Publishers, Dordrecht, the Netherlands. p.286.
Wang G J, Yu E M, Xie J, Yu D G, Li Z F, Luo W, Qiu L J, Zheng Z L. 2015. Effect of C/N ratio on water quality in zero-water exchange tanks and the biofloc supplementation in feed on the growth performance of crucian carp, Carassius auratus. Aquaculture, 443: 98–104, https://doi.org/10.1016/j.aquaculture.2015.03.015.
Wang Q, Garrity G M, Tiedje J M, Cole J R. 2007. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16): 5 261–5 267, https://doi.org/10.1128/AEM.00062-07.
Wei Y F, Liao S A, Wang A L. 2016. The effect of different carbon sources on the nutritional composition, microbial community and structure of bioflocs. Aquaculture, 465: 88–93, https://doi.org/10.1016/j.aquaculture.2016.08.040.
Xu W J, Morris T C, Samocha T M. 2016. Effects of C/N ratio on biofloc development, water quality, and performance of Litopenaeus vannamei juveniles in a biofloc-based, high-density, zero-exchange, outdoor tank system. Aquaculture, 453: 169–175, https://doi.org/10.1016/j.aquaculture.2015.11.021.
Zhao P, Huang J, Wang X H, Song X L, Yang C H, Zhang X G, Wang G C. 2012. The application of bioflocs technology in high-intensive, zero exchange farming systems of Marsupenaeus japonicus. Aquaculture, 354–355: 97–106, https://doi.org/10.1016/j.aquaculture.2012.03.034.
Author information
Authors and Affiliations
Corresponding author
Additional information
Supported by the Yangtze Scholars and Innovative Research Team in University of Ministry of Education of China (No. IRT_17R81) and the Technology Support Project of Tianjin (No. 16YFZCNC00810)
7 Data Availability Statement
The data used to support the findings of this study are available from the corresponding author upon request.
Rights and permissions
About this article
Cite this article
Wang, S., Cui, X., Xu, R. et al. Effect of carbon and nitrogen ratio control on Artemia growth, water quality, biofloc microbial diversity under high salinity and zero-water exchange culture condition. J. Ocean. Limnol. 37, 1768–1776 (2019). https://doi.org/10.1007/s00343-019-8288-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00343-019-8288-5